Supportive Care in Cancer

, Volume 21, Issue 9, pp 2537–2545 | Cite as

Effects of a 12-week home-based exercise program on the level of physical activity, insulin, and cytokines in colorectal cancer survivors: a pilot study

  • Dong Hoon Lee
  • Ji Young Kim
  • Mi Kyung Lee
  • Choae Lee
  • Ji-Hee Min
  • Duck Hyoun Jeong
  • Ji-Won Lee
  • Sang Hui Chu
  • Jeffrey A. Meyerhardt
  • Jennifer Ligibel
  • Lee W. Jones
  • Nam Kyu Kim
  • Justin Y. JeonEmail author
Original Article



The purposes of this study are to examine (1) the feasibility and efficacy of two different home-based exercise protocols on the level of physical activity (PA), and (2) the effect of increased PA via home-based exercise program on biomarkers of colorectal cancer.


Seventeen patients (age 55.18 ± 13.3 years) with stage II–III colorectal cancer completed the 12-week home-based exercise program. Subjects were randomized into either casually intervened home-based exercise group (CIHE) or intensely intervened home-based exercise group (IIHE). The primary outcome was the level of PA. Furthermore, insulin, homeostasis model assessment of insulin resistance, insulin-like growth factor axis, and adipocytokines were measured.


Both CIHE and IIHE program significantly increased the level of PA at 12 weeks compared to its level at baseline (CIHE, 10.00 ± 8.49 vs. 46.07 ± 45.59; IIHE, 12.08 ± 11.04 vs. 35.42 ± 27.42 MET hours per week). Since there was no difference in PA change between groups (p = 0.511), the data was combined in analyzing the effects of increased PA on biomarkers. Increase in PA significantly reduced insulin (6.66 ± 4.58 vs. 4.86 ± 3.48 μU/ml, p = 0.006), HOMA-IR (1.66 ± 1.23 vs. 1.25 ± 1.04, p = 0.017), and tumor necrosis alpha-α (TNF-α 4.85 ± 7.88 vs. 2.95 ± 5.38 pg/ml, p = 0.004), and significantly increased IGF-1 (135.39 ± 60.15 vs. 159.53 ng/ml, p = 0.007), IGF binding protein (IGFBP)-3 (2.67 ± 1.48 vs. 3.48 ± 1.00 ng/ml, p = 0.013), and adiponectin (6.73 ± 3.07 vs. 7.54 ± 3.96 μg/ml, p = 0.015).


CIHE program was as effective as IIHE program in increasing the level of PA, and the increase in PA resulted in significant change in HOMA-IR, IGF-1 axis, TNF-α, and adiponectin levels in stage II–III colorectal cancer survivors.


Colorectal cancer Exercise Insulin resistance IGFs Cytokine 


Research support

National Research Foundation of Korea (NRF) (No. 2011-0004892 to J.Y.J.) and the National R & D program for Cancer Control, Ministry of Health and Welfare, Republic of Korea (1120230 to N.K.K).

Conflict of interest

No author has declared conflicts of interest. The authors have full control of all primary data and that we agree to allow the journal to review the data if required.


  1. 1.
    Agrawal D, Chen T, Irby R, Quackenbush J, Chambers AF, Szabo M, Cantor A, Coppola D, Yeatman TJ (2002) Osteopontin identified as lead marker of colon cancer progression, using pooled sample expression profiling. J Natl Cancer Inst 94:513–521CrossRefGoogle Scholar
  2. 2.
    Arikawa AY, Kurzer MS, Thomas W, Schmitz KH (2010) No effect of exercise on insulin-like growth factor-I, insulin, and glucose in young women participating in a 16-week randomized controlled trial. Cancer Epidemiol Biomarkers Prev 19:2987–2990CrossRefGoogle Scholar
  3. 3.
    Bohlke K, Cramer DW, Trichopoulos D, Mantzoros CS (1998) Insulin-like growth factor-I in relation to premenopausal ductal carcinoma in situ of the breast. Epidemiology 9:570–573CrossRefGoogle Scholar
  4. 4.
    Chokkalingam AP, Pollak M, Fillmore CM, Gao YT, Stanczyk FZ, Deng J, Sesterhenn IA, Mostofi FK, Fears TR, Madigan MP, Ziegler RG, Fraumeni JF Jr, Hsing AW (2001) Insulin-like growth factors and prostate cancer: a population-based case–control study in China. Cancer Epidemiol Biomarkers Prev 10:421–427PubMedGoogle Scholar
  5. 5.
    Craig CL, Marshall AL, Sjostrom M, Bauman AE, Booth ML, Ainsworth BE, Pratt M, Ekelund U, Yngve A, Sallis JF, Oja P (2003) International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc 35:1381–1395CrossRefGoogle Scholar
  6. 6.
    Demark-Wahnefried W, Morey MC, Sloane R, Snyder DC, Miller PE, Hartman TJ, Cohen HJ (2012) Reach out to enhance wellness home-based diet-exercise intervention promotes reproducible and sustainable long-term improvements in health behaviors, body weight, and physical functioning in older, overweight/obese cancer survivors. J Clin Oncol 30:2354–2361CrossRefGoogle Scholar
  7. 7.
    Fairey AS, Courneya KS, Field CJ, Bell GJ, Jones LW, Mackey JR (2003) Effects of exercise training on fasting insulin, insulin resistance, insulin-like growth factors, and insulin-like growth factor binding proteins in postmenopausal breast cancer survivors: a randomized controlled trial. Cancer Epidemiol Biomarkers Prev 12:721–727PubMedGoogle Scholar
  8. 8.
    Friedenreich CM, Neilson HK, Woolcott CG, McTiernan A, Wang Q, Ballard-Barbash R, Jones CA, Stanczyk FZ, Brant RF, Yasui Y, Irwin ML, Campbell KL, McNeely ML, Karvinen KH, Courneya KS (2011) Changes in insulin resistance indicators, IGFs, and adipokines in a year-long trial of aerobic exercise in postmenopausal women. Endocr Relat Cancer 18:357–369CrossRefGoogle Scholar
  9. 9.
    Gomez AM, Martinez C, Fiuza-Luces C, Herrero F, Perez M, Madero L, Ruiz JR, Lucia A, Ramirez M (2011) Exercise training and cytokines in breast cancer survivors. Int J Sports Med 32:461–467CrossRefGoogle Scholar
  10. 10.
    Guadagni F, Roselli M, Martini F, Spila A, Riondino S, D'Alessandro R, Del Monte G, Formica V, Laudisi A, Portarena I, Palmirotta R, Ferroni P (2009) Prognostic significance of serum adipokine levels in colorectal cancer patients. Anticancer Res 29:3321–3327PubMedGoogle Scholar
  11. 11.
    Haydon AM, Macinnis RJ, English DR, Giles GG (2006) Effect of physical activity and body size on survival after diagnosis with colorectal cancer. Gut 55:62–67CrossRefGoogle Scholar
  12. 12.
    Haydon AM, Macinnis RJ, English DR, Morris H, Giles GG (2006) Physical activity, insulin-like growth factor 1, insulin-like growth factor binding protein 3, and survival from colorectal cancer. Gut 55:689–694CrossRefGoogle Scholar
  13. 13.
    Il'yasova D, Colbert LH, Harris TB, Newman AB, Bauer DC, Satterfield S, Kritchevsky SB (2005) Circulating levels of inflammatory markers and cancer risk in the health aging and body composition cohort. Cancer Epidemiol Biomarkers Prev 14:2413–2418CrossRefGoogle Scholar
  14. 14.
    Irwin ML, Varma K, Alvarez-Reeves M, Cadmus L, Wiley A, Chung GG, Dipietro L, Mayne ST, Yu H (2009) Randomized controlled trial of aerobic exercise on insulin and insulin-like growth factors in breast cancer survivors: the Yale Exercise and Survivorship study. Cancer Epidemiol Biomarkers Prev 18:306–313CrossRefGoogle Scholar
  15. 15.
    Jung KW, Park S, Kong HJ, Won YJ, Lee JY, Seo HG, Lee JS (2012) Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2009. Cancer Res Treat 44:11–24CrossRefGoogle Scholar
  16. 16.
    Juul A, Dalgaard P, Blum WF, Bang P, Hall K, Michaelsen KF, Muller J, Skakkebaek NE (1995) Serum levels of insulin-like growth factor (IGF)-binding protein-3 (IGFBP-3) in healthy infants, children, and adolescents: the relation to IGF-I, IGF-II, IGFBP-1, IGFBP-2, age, sex, body mass index, and pubertal maturation. J Clin Endocrinol Metab 80:2534–2542PubMedGoogle Scholar
  17. 17.
    Kim ES, Im JA, Kim KC, Park JH, Suh SH, Kang ES, Kim SH, Jekal Y, Lee CW, Yoon YJ, Lee HC, Jeon JY (2007) Improved insulin sensitivity and adiponectin level after exercise training in obese Korean youth. Obesity (Silver Spring) 15:3023–3030CrossRefGoogle Scholar
  18. 18.
    Lee MK, Jekal Y, Im JA, Kim E, Lee SH, Park JH, Chu SH, Chung KM, Lee HC, Oh EG, Kim SH, Jeon JY (2010) Reduced serum vaspin concentrations in obese children following short-term intensive lifestyle modification. Clin Chim Acta 411:381–385CrossRefGoogle Scholar
  19. 19.
    Liburt NR, Adams AA, Betancourt A, Horohov DW, McKeever KH (2010) Exercise-induced increases in inflammatory cytokines in muscle and blood of horses. Equine Vet J 42(Suppl 38):280–288CrossRefGoogle Scholar
  20. 20.
    Ligibel JA, Giobbie-Hurder A, Olenczuk D, Campbell N, Salinardi T, Winer EP, Mantzoros CS (2009) Impact of a mixed strength and endurance exercise intervention on levels of adiponectin, high molecular weight adiponectin and leptin in breast cancer survivors. Cancer Causes Control 20:1523–1528CrossRefGoogle Scholar
  21. 21.
    Ligibel JA, Giobbie-Hurder A, Olenczuk D, Campbell N, Salinardi T, Winer EP, Mantzoros CS (2009) Impact of a mixed strength and endurance exercise intervention on levels of adiponectin, high molecular weight adiponectin and leptin in breast cancer survivors. Cancer Causes Control 20:1523–1528CrossRefGoogle Scholar
  22. 22.
    Ligibel JA, Meyerhardt J, Pierce JP, Najita J, Shockro L, Campbell N, Newman VA, Barbier L, Hacker E, Wood M, Marshall J, Paskett E, Shapiro C (2012) Impact of a telephone-based physical activity intervention upon exercise behaviors and fitness in cancer survivors enrolled in a cooperative group setting. Breast Cancer Res Treat 132:205–213CrossRefGoogle Scholar
  23. 23.
    Ligibel JA, Meyerhardt J, Pierce JP, Najita J, Shockro L, Campbell N, Newman VA, Barbier L, Hacker E, Wood M, Marshall J, Paskett E, Shapiro C (2012) Impact of a telephone-based physical activity intervention upon exercise behaviors and fitness in cancer survivors enrolled in a cooperative group setting. Breast Cancer Res Treat 132:205–213CrossRefGoogle Scholar
  24. 24.
    Ligibel JA, Partridge A, Giobbie-Hurder A, Campbell N, Shockro L, Salinardi T, Winer EP (2010) Physical and psychological outcomes among women in a telephone-based exercise intervention during adjuvant therapy for early stage breast cancer. J Womens Health (Larchmt) 19:1553–1559CrossRefGoogle Scholar
  25. 25.
    McTiernan A, Sorensen B, Yasui Y, Tworoger SS, Ulrich CM, Irwin ML, Rudolph RE, Stanczyk FZ, Schwartz RS, Potter JD (2005) No effect of exercise on insulin-like growth factor 1 and insulin-like growth factor binding protein 3 in postmenopausal women: a 12-month randomized clinical trial. Cancer Epidemiol Biomarkers Prev 14:1020–1021CrossRefGoogle Scholar
  26. 26.
    Meyerhardt JA, Giovannucci EL, Holmes MD, Chan AT, Chan JA, Colditz GA, Fuchs CS (2006) Physical activity and survival after colorectal cancer diagnosis. J Clin Oncol 24:3527–3534CrossRefGoogle Scholar
  27. 27.
    Meyerhardt JA, Giovannucci EL, Ogino S, Kirkner GJ, Chan AT, Willett W, Fuchs CS (2009) Physical activity and male colorectal cancer survival. Arch Intern Med 169:2102–2108CrossRefGoogle Scholar
  28. 28.
    Meyerhardt JA, Heseltine D, Niedzwiecki D, Hollis D, Saltz LB, Mayer RJ, Thomas J, Nelson H, Whittom R, Hantel A, Schilsky RL, Fuchs CS (2006) Impact of physical activity on cancer recurrence and survival in patients with stage III colon cancer: findings from CALGB 89803. J Clin Oncol 24:3535–3541CrossRefGoogle Scholar
  29. 29.
    Morey MC, Snyder DC, Sloane R, Cohen HJ, Peterson B, Hartman TJ, Miller P, Mitchell DC, Demark-Wahnefried W (2009) Effects of home-based diet and exercise on functional outcomes among older, overweight long-term cancer survivors: RENEW: a randomized controlled trial. JAMA 301:1883–1891CrossRefGoogle Scholar
  30. 30.
    Ngo TH, Barnard RJ, Tymchuk CN, Cohen P, Aronson WJ (2002) Effect of diet and exercise on serum insulin, IGF-I, and IGFBP-1 levels and growth of LNCaP cells in vitro (United States). Cancer Causes Control 13:929–935CrossRefGoogle Scholar
  31. 31.
    Oh EG, Bang SY, Kim SH, Hyun SS, Chu SH, Jeon JY, Im JA, Lee JE, Lee MK (2013) Therapeutic lifestyle modification program reduces plasma levels of the chemokines CRP and MCP-1 in subjects with metabolic syndrome. Biol Res Nurs 15:48–55CrossRefGoogle Scholar
  32. 32.
    Orsatti FL, Nahas EA, Maesta N, Nahas-Neto J, Burini RC (2008) Plasma hormones, muscle mass and strength in resistance-trained postmenopausal women. Maturitas 59:394–404CrossRefGoogle Scholar
  33. 33.
    Ottenbacher AJ, Day RS, Taylor WC, Sharma SV, Sloane R, Snyder DC, Kraus WE, Demark-Wahnefried W (2011) Exercise among breast and prostate cancer survivors—what are their barriers? J Cancer Surviv 5:413–419CrossRefGoogle Scholar
  34. 34.
    Pan HW, Ou YH, Peng SY, Liu SH, Lai PL, Lee PH, Sheu JC, Chen CL, Hsu HC (2003) Overexpression of osteopontin is associated with intrahepatic metastasis, early recurrence, and poorer prognosis of surgically resected hepatocellular carcinoma. Cancer 98:119–127CrossRefGoogle Scholar
  35. 35.
    Rinaldi S, Cleveland R, Norat T, Biessy C, Rohrmann S, Linseisen J, Boeing H, Pischon T, Panico S, Agnoli C, Palli D, Tumino R, Vineis P, Peeters PH, van Gils CH, Bueno-de-Mesquita BH, Vrieling A, Allen NE, Roddam A, Bingham S, Khaw KT, Manjer J, Borgquist S, Dumeaux V, Torhild Gram I, Lund E, Trichopoulou A, Makrygiannis G, Benetou V, Molina E, Donate Suarez I, Barricarte Gurrea A, Gonzalez CA, Tormo MJ, Altzibar JM, Olsen A, Tjonneland A, Gronbaek H, Overvad K, Clavel-Chapelon F, Boutron-Ruault MC, Morois S, Slimani N, Boffetta P, Jenab M, Riboli E, Kaaks R (2010) Serum levels of IGF-I, IGFBP-3 and colorectal cancer risk: results from the EPIC cohort, plus a meta-analysis of prospective studies. Int J Cancer 126:1702–1715PubMedGoogle Scholar
  36. 36.
    Rittling SR, Chambers AF (2004) Role of osteopontin in tumour progression. Br J Cancer 90:1877–1881CrossRefGoogle Scholar
  37. 37.
    Smart NA, Steele M (2011) The effect of physical training on systemic proinflammatory cytokine expression in heart failure patients: a systematic review. Congest Heart Fail 17:110–114CrossRefGoogle Scholar
  38. 38.
    Suzuki S, Kojima M, Tokudome S, Suzuki K, Ozasa K, Ito Y, Inaba Y, Tajima K, Nakachi K, Watanabe Y, Tamakoshi A (2009) Insulin-like growth factor (IGF)-I, IGF-II, IGF binding protein-3, and risk of colorectal cancer: a nested case–control study in the Japan Collaborative Cohort study. Asian Pac J Cancer Prev 10(Suppl):45–49PubMedGoogle Scholar
  39. 39.
    Vallance J, Lesniak SL, Belanger LJ, Courneya KS (2010) Development and assessment of a physical activity guidebook for the Colon Health and Life-Long Exercise Change (CHALLENGE) trial (NCIC CO.21). J Phys Act Health 7:794–801CrossRefGoogle Scholar
  40. 40.
    Volkova E, Willis JA, Wells JE, Robinson BA, Dachs GU, Currie MJ (2011) Association of angiopoietin-2, C-reactive protein and markers of obesity and insulin resistance with survival outcome in colorectal cancer. Br J Cancer 104:51–59CrossRefGoogle Scholar
  41. 41.
    Wei EK, Ma J, Pollak MN, Rifai N, Fuchs CS, Hankinson SE, Giovannucci E (2005) A prospective study of C-peptide, insulin-like growth factor-I, insulin-like growth factor binding protein-1, and the risk of colorectal cancer in women. Cancer Epidemiol Biomarkers Prev 14:850–855CrossRefGoogle Scholar
  42. 42.
    Wolpin BM, Meyerhardt JA, Chan AT, Ng K, Chan JA, Wu K, Pollak MN, Giovannucci EL, Fuchs CS (2009) Insulin, the insulin-like growth factor axis, and mortality in patients with nonmetastatic colorectal cancer. J Clin Oncol 27:176–185CrossRefGoogle Scholar
  43. 43.
    Yu H, Rohan T (2000) Role of the insulin-like growth factor family in cancer development and progression. J Natl Cancer Inst 92:1472–1489CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Dong Hoon Lee
    • 1
  • Ji Young Kim
    • 1
  • Mi Kyung Lee
    • 1
  • Choae Lee
    • 1
  • Ji-Hee Min
    • 1
  • Duck Hyoun Jeong
    • 2
  • Ji-Won Lee
    • 3
  • Sang Hui Chu
    • 4
  • Jeffrey A. Meyerhardt
    • 5
  • Jennifer Ligibel
    • 5
  • Lee W. Jones
    • 6
  • Nam Kyu Kim
    • 2
  • Justin Y. Jeon
    • 1
    • 7
    Email author
  1. 1.Department of Sport and Leisure StudiesYonsei University College of EducationSeoulKorea
  2. 2.Department of SurgeryYonsei University College of MedicineSeoulKorea
  3. 3.Department of Family MedicineYonsei University College of MedicineSeoulKorea
  4. 4.Department of Clinical Nursing Science, Nursing Policy and Research Institute, Biobehavioral Research CenterYonsei University College of NursingSeoulKorea
  5. 5.Department of Medical Oncology, Dana Farber Cancer InstituteHarvard Medical SchoolBostonUSA
  6. 6.Duke University Medical CenterDurhamUSA
  7. 7.Department of Sport and Leisure StudiesYonsei UniversitySeoulKorea

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